×

Sterile males and females can synergistically suppress wild pests targeted by sterile insect technique. (English) Zbl 1472.92262

Summary: The sterile insect technique (SIT) involves periodically releasing artificially sterilized insects to inhibit normal mating between wild insect pests, ultimately resulting in the eradication of wild pest populations. It has often been discussed whether releasing either one sex, mainly males, of sterile insects (i.e., a unisexual release) can enhance the pest-control effect of the SIT more than releasing both sexes (i.e., a bisexual release). We constructed a mathematical model to examine the contribution of sterile males and females to the pest-control effect and the synergy between them. We consider that males seek out and court females in accord with their own female searching ability and preference, and that females subsequently choose one male from among males courting them in accordance with their own preference. Using this model, we compared the pest-control effect of bisexual and unisexual release, focusing on the difference in mating systems of the targeted insects. We showed that for swarm-type mating systems (with few courtship chances with higher encounter rates), bisexual release was the most effective, irrespective of the relative female searching ability between wild and sterile males. In this case, sterile females indirectly reduce wild females mating with either male by absorbing courtship from both wild and sterile males. By contrast, bisexual release is the most effective for scramble-type mating systems (more courtship chances with lower encounter rates) only when the female searching ability of sterile males is lower than that of wild males. In this case, sterile females absorb courtship from males with higher searching abilities. Therefore, the net impact of sterile females depends on the difference in sexual performance between wild and sterile males. Because the sexual performance of sterile insects is often degraded during the process of sterilization, we suggest that bisexual release can be a compatible measure to efficiently suppress wild pest populations.

MSC:

92D45 Pest management
Full Text: DOI

References:

[1] Ailam, G.; Galun, R., Optimal sex ratio for the control of insects by the sterility method, Ann. Entomol. Soc. Am., 60, 41-43 (1967)
[2] Bakri, A.; Mehta, K.; Lance, D., Sterilizing insects with ionizing radiation, (Dyck, V. A.; Hendrichs, J.; Robinson, A. S., Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management (2005), Springer: Springer Dordrecht), 233-268
[3] Barclay, H. J., Mathematical models for the use of sterile insects, (Dyck, V. A.; Hendrichs, J.; Robinson, A. S., Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management (2005), Springer: Springer Dordrecht), 147-174
[4] Bloem, K.; Bloem, S.; Rizzo, N.; Chambers, D., Female medfly refractory period: effect of male reproductive status, (Aluja, M.; Liedo, P., Fruit flies (1993), Springer-Verlag, New York: Springer-Verlag, New York Biology and management), 189-190
[5] Bonduriansky, R., The evolution of male mate choice in insects: A synthesis of ideas and evidence, Biol. Rev., 76, 3, 305-339 (2001)
[6] Calkins, C. O.; Parker, A. G., Sterile insect quality, (Dyck, V. A.; Hendrichs, J.; Robinson, A. S., Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management (2005), Springer: Springer Dordrecht), 269-296
[7] Edward, D. A.; Chapman, T., The evolution and significance of male mate choice, Trends Ecol. Evol., 26, 12, 647-654 (2011)
[8] Elias, D. O.; Sivalinghem, S.; Mason, A. C.; Andrade, M. C.B.; Kasumovic, M. M., Mate-guarding courtship behaviour: tactics in a changing world, Anim. Behav., 97, 25-33 (2014)
[9] Evans, T. P.; Bishop, S. R., A spatial model with pulsed releases to compare strategies for the sterile insect technique applied to the mosquito Aedes aegypti, Math. Biosci., 254, 6-27 (2014) · Zbl 1323.92180
[10] Franz, G., Genetic sexing strains in Mediterranean fruit fly, an example for other species amenable to large-scale rearing for the sterile insect technique, (Dyck, V. A.; Hendrichs, J.; Robinson, A. S., Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management (2005), Springer: Springer Dordrecht), 427-451
[11] Fried, M., Determination of sterile-insect competitiveness, J. Econ. Entomol., 64, 869-872 (1971)
[12] Gröning, J.; Hochkirch, A., Reproductive interference between animal species, Q. Rev. Biol., 83, 257-282 (2008)
[13] Hendrichs, J.; Robinson, A. S.; Cayol, J. P.; Enkerlin, W., Medfly areawide sterile insect technique programmes for prevention, suppression or eradication: The importance of mating behavior studies, Florida Entomol., 85, 1, 1-13 (2002)
[14] Hight, S. D.; Carpenter, J. E.; Bloem, S.; Bloem, K. A., Developing a sterile insect release program for Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae): Effective overflooding ratios and release-recapture field studies, Envion. Entomol., 34, 4, 850-856 (2005)
[15] Himuro, C.; Ikegawa, Y.; Honma, A., Males use accessory gland substances to inhibit remating by females in West Indian sweetpotato weevil (Coleoptera: Curculionidae), Ann. Entomol. Soc. Am., 110, 374-380 (2017)
[16] Honma, A.; Kumano, N.; Noriyuki, S., Killing two bugs with one stone: A perspective for targeting multiple pest species by incorporating reproductive interference into sterile insect technique, Pest Manag. Sci., 75, 3, 571-577 (2018)
[17] Ikegawa, Y.; Himuro, C., Limited mobility of target pests crucially lowers controllability when sterile insect releases are spatiotemporally biased, J. Theor. Biol., 421, 93-100 (2017) · Zbl 1370.92173
[18] Itô, Y., History and successful example of sterile insect technique in the world (in Japanese), (Itô, Y., Sterile Insect Technique: Eradication Technique for Invasive Species (2008), Kaiyusha: Kaiyusha Tokyo), 1-17
[19] Klassen, W.; Curtis, C. F., History of the sterile insect technique, (Dyck, V. A.; Hendrichs, J.; Robinson, A. S., Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management (2005), Springer: Springer Dordrecht), 3-36
[20] Knipling, E. F., Possibilities of insect population control through the use of sexually sterile males, J. Econom. Entomol., 48, 443-448 (1955)
[21] Knipling, E. F., Sterile-male method of population control, Science, 130, 902-904 (1959)
[22] Kraaijeveld, K.; Katsoyannos, B. I.; Stavrinides, M.; Kouloussis, N. A.; Chapman, T., Remating in wild females of the Mediterranean fruit fly, Ceratitis capitata, Anim. Behav., 69, 4, 771-776 (2005)
[23] Kumano, N.; Kohama, T.; Ohno, S., Effect of irradiation on dispersal ability of male sweetpotato weevils (Coleoptera: Brentidae) in the field, J. Econ. Entomol., 100, 730-736 (2007)
[24] Kuno, E., Competitive exclusion through reproductive interference, Res. Popul. Ecol., 34, 2, 275-284 (1992)
[25] Lawson, F. R., Theory of control of insect populations by sexually sterile males, Ann. Entomol. Soc. Am., 60, 713-722 (1967)
[26] Matsuyama, T., Eradication project of the sweet potato weevil, Cylas formicarius (Fabricius), in Kume Island, Okinawa, Japan, Inform. Pests Japan, 100, 7-8 (2013), (in Japanese)
[27] McInnis, D. O.; Wong, T. T.Y.; Tam, S. Y.T., Mediterranean fruit fly (Diptera: Tephritidae): Suppression efficiencies of unisexual and bisexual sterilized release populations in field cages, Ann. Entomol. Soc. Am., 79, 931-937 (1986)
[28] McInnis, D. O.; Tam, S. Y.T.; Grace, C.; Miyashita, D., Population suppression and sterility rates induced by variable sex-ratio, sterile insect releases of Ceratitis capitata (Diptera: Tephritidae) in Hawaii, Ann. Entomol. Soc. Am., 86, 231-240 (1994)
[29] Ohishi, T.; Matsuyama, T.; Himuro, C.; Ohno, S.; Sadoyama, Y.; Kinjo, M.; Honma, A., The eradication projects and the phytosanitary measures for quarantine pests in Okinawa, (Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management on Key Crop (2018)), 31-48
[30] Parker, A. G., Mass-rearing for sterile insect release, (Dyck, V. A.; Hendrichs, J.; Robinson, A. S., Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management (2005), Springer: Springer Dordrecht), 209-232
[31] Pérez-Staples, D.; Shelly, T. E.; Yuval, B., Female mating failure and failure of ’mating’ in sterile insect programs, Entomol. Exp. Appl., 146, 66-78 (2013)
[32] Rendón, P.; McInnis, D.; Lance, D.; Stewart, J., Medfly (Diptera: Tephritidae) genetic sexing: Large scale field comparison of males-only and bisexual sterile fly releases in Guatemala, J. Econ. Entomol., 97, 5, 1547-1553 (2004)
[33] Suckling, D. M.; Hackett, J. K.; Chhagan, A.; Barrington, A.; El-Sayed, A. M., Effect of irradiation on female painted apple moth Teia anartoides (Lep., Lymantriidae) sterility and attractiveness to males, J. Appl. Entomol., 130, 3, 167-170 (2006)
[34] Sullivan, R. T., Insect swarming and mating, Fla. Entomol., 97, 1547-1553 (1981)
[35] Thornhill, R.; Alcock, J., The Evolution of Insect Mating Systems (1983), Harvard University Press: Harvard University Press Cambridge, MA
[36] Vreysen, M. J.B.; Barclay, H. J.; Hendrichs, J., Modeling of preferential mating in areawide control programs that integrate the release of stains of sterile males only or both sexes, Ann. Entomol. Soc. Am., 99, 607-616 (2006)
[37] Whitten, M. J.; Taylor, W. C., A role for sterile females in insect control, J. Econ. Entomol., 63, 269-272 (1970)
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.